Abstract
In the mammalian cochlea, specialized ribbon-type synapses between sensory inner hair cells (IHCs) and postsynaptic spiral ganglion neurons ensure the temporal precision and indefatigability of synaptic sound encoding. These high-through-put synapses are presynaptically characterized by an electron-dense projection—the synaptic ribbon—which provides structural scaffolding and tethers a large pool of synaptic vesicles. While advances have been made in recent years in deciphering the molecular anatomy and function of these specialized active zones, the developmental assembly of this presynaptic interaction hub remains largely elusive. In this review, we discuss the dynamic nature of IHC (pre-) synaptogenesis and highlight molecular key players as well as the transport pathways underlying this process. Since developmental assembly appears to be a highly dynamic process, we further ask if this structural plasticity might be maintained into adulthood, how this may influence the functional properties of a given IHC synapse and how such plasticity could be regulated on the molecular level. To do so, we take a closer look at other ribbon-bearing systems, such as retinal photoreceptors and pinealocytes and aim to infer conserved mechanisms that may mediate these phenomena.
Highlights
Hearing relies on the ultrafast, temporally-precise and frequency-specific encoding of sound into neural signals
The cochlea harbors the highly structured sensory epithelium—the organ of Corti—which consists of three rows of electromotile outer hair cells (OHCs) and one row of sensory inner hair cells (IHCs) that are organized in a tonotopic manner (Figure 1B,C)
While OHCs play a key role in active cochlear amplification, IHCs are the true sensory receptor cells that perform the challenging task of synaptic sound encoding, that is, the transformation of a physical stimulus into neural code at their ribbon synapses with postsynaptic spiral ganglion neurons (SGNs)
Summary
Hearing relies on the ultrafast, temporally-precise and frequency-specific encoding of sound into neural signals. While OHCs play a key role in active cochlear amplification, IHCs are the true sensory receptor cells that perform the challenging task of synaptic sound encoding, that is, the transformation of a physical stimulus into neural code at their ribbon synapses with postsynaptic spiral ganglion neurons (SGNs). While the knowledge of the functional role and molecular anatomy of mature IHC ribbons is ever expanding, information on the early assembly and developmental maturation of auditory ribbon-type AZs prior to hearing onset (~p12 in mice; [25]) remains comparably scarce Despite of their functional implications, other important physiological processes—such as structural plasticity—are still elusive to date, largely due to the technical difficulties in simultaneously visualizing, while adequately stimulating, the tissue in vivo and even in vitro.
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